Environmental Health Perspectives Volume
103, Supplement 4, May 1995
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Effects of Polychlorinated Dibenzo-p-dioxins and Dibenzofurans
on Nesting Wood Ducks (Aix Sponsa) at Bayou Meto, Arkansas
Donald H. White1 and David J. Hoffman2
1National Biological Service, University of Georgia, Athens,
Georgia; 2National Biological Service, Patuxent Environmental
Science Center, Laurel, Maryland
Abstract
Wood ducks (Aix sponsa) nesting along Bayou Meto downstream from
a hazardous waste site in central Arkansas were contaminated with polychlorinated
dibenzo-p-dioxins (PCDDs) and dibenzofurans (PCDFs). Residues in
eggs, based on 2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents (TCDD-EQ),
ranged up to 611 parts per trillion (ppt), and egg arithmetic means were
90-fold higher at the site nearest the point source compared with a reference
site. We monitored productivity of wood ducks in artificial nest boxes at
three sites on the bayou and at a reference site on a separate drainage
during 1988-1990. Productivity was suppressed (p<0.05) at the
bayou sites compared with the reference site, and egg TCDD-EQs were inversely
correlated (p<0.001) with productivity in corresponding nests.
The threshold range of toxicity, where reduced productivity was evident
in wood ducks (based on TCDD-EQs), was >20 to 50 ppt. Oxidative stress
and teratogenic effects occurred in ducklings at the more contaminated nesting
sites nearest the point source. These findings suggest that wood ducks may
be more sensitive to PCDD and PCDF contamination than some other aquatic
birds and could serve as an indicator species for monitoring biological
impacts from these contaminants. -- Environ Health Perspect 103(Suppl
4):00-00 (1995)
Key words: polychlorinated dibenzo-p-dioxins, dibenzofurans,
reproductive impairment, Aix sponsa, contaminants, Arkansas, wood
ducks
This paper was presented at the Conference on Environmentally
Induced Alterations in Development: A Focus on Wildlife held 10-12 December
1993 in Racine, Wisconsin.
The U.S. Environmental Protection Agency provided funding
for chemical analyses of samples.
Address correspondence to Dr. Donald H. White, U.S. Department
of the Interior, National Biological Service, Warnell School of Forest
Resources, The University of Georgia, Athens, GA. Telephone (706) 542-1609.
Fax (706) 542-1235.
Introduction
Bayou Meto, a major drainage system in central Arkansas, is contaminated
with polychlorinated dibenzo-p-dioxins (PCDDs) and dibenzofurans
(PCDFs). The U.S. Environmental Protection Agency (U.S. EPA) identified
a former chemical plant that manufactured the herbicide 2,4,5-T as the source
of contamination and subsequently included the area on the national priorities
list of hazardous waste sites in 1982. Preliminary investigations by the
Arkansas Game and Fish Commission (AGFC) revealed elevated levels of PCDDs
in waterfowl collected downstream from the chemical plant. Residues of 2,3,7,8-tetra-CDD
in wood duck (Aix sponsa) carcasses there ranged up to 510 parts
per trillion (ppt) wet weight, but no PCDDs were found in wood ducks from
a reference site on a separate drainage (GA Perkins, SC Yaich, unpublished
report). Field studies have implicated PCDDs as contributing factors in
reproductive failure of certain aquatic birds (1,2), and we reported
similar negative effects in wood ducks nesting at Bayou Meto, Arkansas (3).
Here we review our earlier results and provide additional evidence of PCDD
and PCDF effects on wood ducks based on liver enzyme and thiol status assays.
Materials and Methods
Bayou Meto flows southeast through agricultural lands in central Arkansas
for about 110 km; its banks consist of a narrow strip (100-200 m wide) of
bottomland habitat that is homogeneous throughout its length. The adjacent
croplands are a major wintering area for waterfowl, mainly mallards (Anas
platyrhynchos). Wood ducks nest in natural cavities in large trees along
the stream. To facilitate monitoring of wood duck productivity, we erected
30 wooden nest boxes with metal predator guards at each of three sites 9,
17, and 58 km downstream from the point source and at one site on the White
River National Wildlife Refuge (reference site) 111 km away. These four
sites were the same where wood ducks were collected earlier by AGFC, so
we had prior knowledge of PCDD and PCDF contamination there.
Refer to our previous report (3) for detailed methods and procedures.
Briefly, during 1988 to 1990 we visited nest boxes weekly beginning in mid-February
each year. When a new nest was found, one fresh egg was taken for chemical
analysis. These were kept refrigerated until the end of the nesting season
(mid-July) each year and then prepared for analysis. Triangle Laboratories,
Inc. (Durham, NC) performed the chemical analyses of egg contents according
to U.S. EPA Method 8290 (4). Although specific isomers were quantified,
we only report homologue totals here. Because Bayou Meto flows through croplands,
samples also were analyzed for organochlorine pesticides (OCs) and polychlorinated
biphenyls (PCBs) as possible contributors to reproductive impairment. Eggs
in nests that failed to hatch were collected and examined for embryonic
anomalies. In addition, during the nesting season of 1989, we collected
one duckling on the day of hatch from 16 nests at sites 1, 2, and 3 for
liver enzyme and thiol status assays (5); these assays indicate oxidative
stress from contaminants such as PCDDs (6,7). We were unable to get
ducklings from the reference site for this purpose. For comparing cumulative
effects of PCDDs and PCDFs in samples among sites, we calculated 2,3,7,8-tetra-CDD
toxicity equivalents (TCDD-EQ) (8) using factors developed by U.S.
EPA (9).
We combined data from all years because no differences were detected
in residue means, hatching success, or duckling production within sites
among years. For among site comparisons, we used chi-square contingency
tables (nest success and hatching success) and analysis of variance with
Tukey's multiple comparison procedure (residues and duckling production).
We used correlation analysis to test relationships between egg residues
and reproductive variables. We used t-tests to compare liver enzyme
levels in ducklings; data from sites 1 and 2 were combined and compared
with site 3. Null hypotheses for all tests were rejected at p
0.05.
Results and Discussion
Data are scarce on PCDD and PCDF contamination in wild birds. Most reports
are of residues in eggs of aquatic birds from the Great Lakes (10-12)
where elevated concentrations up to 1200 ppt have been found. Some eggs
from our three bayou sites, especially sites 1 and 2 (9 and 17 km downstream),
had elevated PCDD and PCDF residues compared to those from the reference
site, and generally, as distance from the point source increased, residues
in eggs decreased (Table 1). On average, the highly toxic 2,3,7,8-TCDD isomer
accounted for 70% of the total TCDD detected. Variable residue concentrations
were not unexpected because wood ducks are highly mobile and may cover a
wide range of habitats. Even resident species with extremely small home
ranges accumulate pollutants differently (13). Only a few of our
samples contained detectable levels of DDE, dieldrin, and heptachlor epoxide
(all <1 ppm), and we believe these concentrations are biologically insignificant.
No other OCs or PCBs were detected.
All nests at site 3 and the reference site hatched at least one egg,
but nest success at sites 1 and 2 was reduced (Table 2). Hatching success
was lowest at site 1 nearest the point source and increased downstream,
as did duckling production. In contrast, mean egg TCDD-EQs (representing
cumulative toxicity) were 90-fold higher at site 1 than at the reference
site and were negatively correlated (p<0.001) with hatching success
and duckling production. In other words, as toxicity in eggs decreased,
productivity increased, regardless of where the eggs were laid. We arbitrarily
grouped egg TCDD-EQs to establish a threshold range of toxicity where some
reduction in productivity was evident. Nest success was normal until egg
TCDD-EQs exceeded 20 ppt (Table 3). Hatching success was reduced in clutches
with TCDD-EQs of >5 to 20 ppt, but these nests still produced nearly
as many live ducklings as the optimal group. However, nest success, hatching
success, and duckling production all dropped 30 to 40% when egg TCDD-EQs
were in the range of >20 to 50 ppt, compared to the optimal group.
Because 2,3,7,8-TCDD is a known teratogen (14), we examined 250
failed eggs for overt embryonic anomalies. Only about 35% (n=87)
contained discernable embryos, and the rest were desiccated or addled. Six
eggs from a 10-egg clutch in 1989 had full-term embryos with lower bill
deformities; at least two of these also exhibited subcutaneous edema of
the head and neck. A deformed duckling from this clutch had a TCDD-EQ value
of 42 ppt. Similar effects were produced in chickens when the eggs were
injected with 10 pg/g 2,3,7,8-TCDD (15).
Alterations in hepatic glutathione status, as well as increased activities
of associated enzymes, have been related to exposure to oxidative stress
by environmental contaminants including certain halogenated hydrocarbons,
such as PCDDs and PCDFs (5-7). In our study, there was evidence of
increased oxidative stress in duckling livers from the highly contaminated
sites (sites 1 and 2) compared with site 3 where contamination was much
lower (Table 4). Small sample sizes curbed the analysis, but significant
differences were detected between some site comparisons. Glutathione-peroxidase
activity, oxidized glutathione concentration, and the ratio of oxidized
versus reduced glutathione were all elevated at combined sites 1 and 2 compared
with site 3.
We conclude that wood ducks may be more sensitive to PCDD and PCDF exposure
than some other avian species and therefore may be a suitable indicator
for contamination of this type. Great blue herons (Ardea herodias)
reproduced normally with a mean of 92 ppt 2,3,7,8-TCDD in eggs, but not
with 252 ppt (16). Kubiak et al. (12) believed PCBs were primarily
responsible for reproductive failure in Forster's terns (Sterna forsteri),
even though eggs had a median level of 37 ppt 2,3,7,8-TCDD. Exposure to
PCDDs decreased egg production in ring-necked pheasants (Phasianus colchicus)
(17), but clutch sizes of wood ducks were normal (18) in our
study, as was egg size (19). Although most of the PCDD and PCDF homologues
in eggs were negatively correlated with reproductive variables, TCDD-EQs
provided the highest correlations. Thus, reproductive failure in our study
probably resulted from cumulative effects rather than from a single compound,
as suggested in other studies (7,12,20,21).
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